Biomechanical Comparison of Different Surgical Strategies for Skip-level Cervical Degenerative Disc Disease

Abstract

Study Design.

We constructed finite element (FE) models of the cervical spine consisting of C2-C7 and predicted the biomechanical effects of different surgical procedures and instruments on adjacent segments, internal fixation systems, and the overall cervical spine through FE analysis.

Objective.

To compare the biomechanical effects between the zero-profile device and cage-plate device in skip-level multistage anterior cervical discectomy and fusion (ACDF).

Summary of Background Data.

ACDF is often considered the standard treatment for degenerative cervical spondylosis. However, the selection of surgical methods and instruments in cases of skip-level cervical degenerative disk disease is still controversial.

Materials and Methods.

Three FE models were constructed, which used noncontiguous 2-level Zero-P (NCZP) devices for C3/4 and C5/6, a noncontiguous 2-level cage-plate (NCCP) for C3/4 and C5/6, and a contiguous 3-level cage-plate (CCP) for C3/6. Simulate daily activities in ABAQUS. The range of motion (ROM), von Mises stress distribution of the endplate and internal fixation system, and intervertebral disk pressure (IDP) of each model were recorded and compared.

Results.

Similar to the stress of the cortical bone, the maximum stress of the Zero-P device was higher than that of the CP device for most activities. The ROM increments of the superior, inferior, and intermediate segments of the NCZP model were lower than those of the NCCP and CCP models in many actions. In terms of the IDP, the increment value of stress for the NCZP model was the smallest, whereas those of the NCCP and CCP models were larger. Similarly, the increment value of stress on the endplate also shows the minimum in the NCZP model.

Conclusions.

Noncontiguous ACDF with zero profile can reduce the stress on adjacent intervertebral disks and endplates, resulting in a reduced risk of adjacent segment disease development. However, the high cortical bone stress caused by the Zero-P device may influence the risk of fractures.

Skip-level cervical degenerative disk disease (CDDD) is a special type of multilevel CDDD that includes one or more normal or less involved segments among the lesion levels.¹ Anterior cervical discectomy and fusion (ACDF) is often considered the standard treatment for degenerative cervical spondylosis.² The conventional ACDF surgery can provide extensive anterior exposure, direct decompression of the nerve tissue, and reconstruction of the cervical spine in a sagittal position through intraoperative placement of an interbody fusion cage and plate.³ It has the advantages of a small incision, short operative time, and simple operation in the treatment of single-segment and continuous two-segment CDDD.^4,5 However, the selection of surgical methods and instruments in cases of skip-level CDDD is still controversial.^1,6–8 The affected segments can be operated separately to preserve the normal motion of the middle segment, or the entire segment can be operated to increase stability and prevent secondary surgery due to degeneration of the middle segment. Clinicians suggested that the incidence of symptomatic adjacent segment disease (ASD) after ACDF was between 9% and 17% and considered that ASD was related to plate placement in traditional anterior surgery.^9,10 Although the pathogenesis of this secondary ASD remains unclear, subsequent biomechanical studies suggest that the limited range of motion (ROM) of the surgical segment leading to abnormal intervertebral disk pressure (IDP) in the adjacent segment may be the main cause of ASD.^11,12

The zero-profile (Zero-P) device is a novel device suitable for ACDF surgery because it reduces the use of plates and has the advantage of reduced exposure and simplified multilevel procedures.^4,13,14 In a previous biomechanical study of the Zero-P device by Li et al,⁴ it was shown that in a single-segment ACDF, the stress increment of the endplate and intervertebral disk in the Zero-P fusion model was slightly lower than that in a cage plate (CP). However, the CP provided better segmental stability than Zero-P. Furthermore, the plate can be used as a framework to resist axial compression, connecting multiple vertebrae and instruments as one unit and reducing subsequent loss of intervertebral height and lordosis, thereby reducing the occurrence of progressive cervical degeneration.^15,16

In recent years, more and more clinical workers have paid attention to patients with skip-level CDDD and compared the clinical efficacy of different surgical methods. However, the evidence of biomechanical manifestations is still under investigation. Thus, in this study, we constructed a finite element (FE) model of the cervical spine consisting of C2-C7 and predicted the biomechanical effects of different surgical procedures and instruments on adjacent segments, internal fixation systems, and the overall cervical spine through FE analysis.

MATERIALS AND METHODS

FE model of Cervical Vertebra (C2-C7) in Healthy Adults

The FE model of the cervical vertebrae (C2-C7) in healthy adults in this study was designed based on a 26-year-old male volunteer with no history of trauma or bone fractures. The absence of cervical spondylosis in this volunteer was confirmed by radiography. The volunteer was recruited in November 2020 and signed an informed consent form. The study was approved by the ethics committee. Accordingly, a 64-slice spiral CT scanner (Siemens, Erlangen, Germany) was used to obtain Digital Imaging and Communications in Medicine (DICOM) images at the level C2-C7 vertebrae.¹⁷ In addition, the Mimics 20.0 (Materialise Inc., Leuven, Belgium) was used to create a 3D vertebral surface model of the C2-C7 area and generate an STL format file from the DICOM images. Further, 3-Matic 12.0 (Materialise Inc.) was used to construct the intervertebral disk, nucleus pulposus, and other structures.¹⁸ Accordingly, it was imported into reverse engineering software (Geomagic Studio 12.0, Geomagic Inc., USA) and materialized using processing methods, including smoothing, construction patches, and grilles. The meshing of the FE model was constructed using Hypermesh 2017 (Altair Engineering, Troy, Michigan, USA). Finally, all models were imported into Abaqus 2020 (Abaqus Inc., USA) for the FE analysis.¹⁹

The intact C2-C7 FE model is shown in Fig. 1. Linear elastic materials were used for the vertebral body and the intervertebral disk. A tetrahedral mesh was used in the vertebral body, and a hexahedral mesh was used in the intervertebral disk. The element type of vertebral body uses C3D4 with 0.5 mm mesh size, and the intervertebral disk uses C3D8R element with a majority of 1 mm mesh size. The total number of elements in the intact model was 2,227,359. The facet joint and cartilage endplate were simulated by using a shell element with a thickness of 0.2 mm and 0.4 mm, respectively. The nucleus pulposus accounts for one-third of the intervertebral volume, and the annulus fibrosus consists of an annulus fibrosus matrix and fibers. The inclination of the annular fibers relative to the horizontal plane is between 15° and 45°.^20,21

Figure 1.

The intact finite element model of the cervical vertebrae (C2-C7).

The model simulated ligaments, including the anterior longitudinal ligament (ALL), posterior longitudinal ligament (PLL), ligamentum flavum (LF), interspinous ligament (ISL), and articular capsule ligament (CL). The annulus fibrosus and the intervertebral ligaments (ALL, PLL, LF, ISL, CL) were modeled as tension-only truss elements. Further, the contact between the facet joints was designated as frictionless sliding.²² The material properties used in the FE model (Table 1) were derived from relevant literature.^17,19

TABLE 1.

Material Properties Defined in the T8–S Finite Element Model

Component	Young’s modulus (MPa)	Poisson’s ratio	Cross-sectional area (mm2)
Bony structures
Cortical bone	12,000	0.29	—
Cancellous bone	450	0.29	—
Posterior structure	3,500	0.29	—
Facet cartilage	10	0.4	—
Intervertebral disk
Annulus fibre	450	0.45	0.15
Annulus ground	3.4	0.4	—
Nucleus pulposus	1	0.49	—
Endplate	500	0.4	—
Ligaments
ALL	15	—	11.1
PLL	10	—	11.3
LF	5	—	46
ISL	4	—	12
CL	7	—	42.2
Implants
Ti	110,000	0.3	—
PEEK cage	3000	0.3	—
Bone graft	450	0.29	—

ALL indicates anterior longitudinal ligament; CL, cystic ligament; ISL, interspinous ligament; LF, ligamentum flavum; PLL, posterior longitudinal ligament.

Validation of the FE Model

The lower surface of the C7 vertebral body was fixed with six df, and the odontoid surface of C2 was coupled with the reference point at the upper 2 mm. Furthermore, a pure moment of 1.0 Nm was applied at this reference point to simulate the movement of flexion, extension, lateral bending, and rotation of the cervical vertebra. The ROM of each segment was measured and compared using previously published in vitro²³ and FE analysis.^17,24

FE Postoperative Model

The C3/4 and C5/6 intervertebral disks were removed and a zero-profile device or a CP was implanted for fixation to simulate the postoperative state of CDDD after ACDF. In this regard, three FE models were constructed, which used noncontiguous 2-level zero-profile (NCZP) devices for C3/4 and C5/6, a noncontiguous 2-level CP (NCCP) for C3/4 and C5/6, and a contiguous 3-level CP (CCP) for C3/6. In the FE surgical models, the zero-profile and CP systems were tied to the vertebral body using screws. To date, three FE ACDF models have been developed successfully (Fig. 2).

Figure 2.

(A) Noncontiguous 2-level zero-profile (NCZP) devices for C3/4 and C5/6; (B) a noncontiguous 2-level CP (NCCP) for C3/4 and C5/6; (C) a contiguous 3-level CP (CCP) for C3/6; (D) zero-profile device; and (E)CP device.

FE Simulation Analysis

The lower surface of C7 was fixed, and the upper surface of the C2 odontoid process was coupled with the reference point.²⁵ An axial compression force of 50 N was applied to the three postoperative FE models to simulate head gravity, and a moment of 1 Nm was applied to simulate flexion, extension, lateral bending, and axial rotation during daily activities.^17,26 The ROM, von Mises stress distribution of the endplate and internal fixation system and IDP of each model were recorded and compared.

RESULTS

Validation of the FE Model

The ROM of our intact FE model for most of the segments was in the range of the cadaveric experiment data (Fig. 3). Except for the C6-7 ROM in axial rotation, the other segments did not exceed 10% of the standard range. The C6-7 ROM of our model in axial rotation is 4.95°, which was 1.25° larger than that of the cadaveric experiment data. Nevertheless, this value was still within the range of the two FE models’ data (4.72°– 5.24°). In lateral bending, both Hua’s¹⁷ and Lee’s²⁶ finite element models showed a tendency toward a higher rigidity. Our models were closer to the range of mobility of the Panjabi’s²³ cadaver experiment. After validation, our FE model conforms to the kinematic characteristics of the cervical spine and could be used to analyze the biomechanical effects of ACDF in the cervical spine.

Figure 3.

Comparison of level-by-level ROM for intact finite element model between in vitro experimental and reported data in flexion/extension, lateral bending, and axial rotation at 1 Nm.

ROM in the Cervical Spine After ACDF

The segmental ROM values of the FE models of ACDF using noncontiguous 2-level zero-profile devices, a noncontiguous 2-level CP, and a contiguous 3-level CP are listed in Fig. 4, respectively. For the fused segments (C3-C4 and C5-6 of all FE surgical models and C4-C5 of the CCP model), the segmental ROM was significantly lower than that of the intact model. Moreover, the ROM values of flexion-extension, lateral bending, and axial rotation of the fused segment of the NCZP model were slightly larger than those of the two-cage plate models. Furthermore, for the nonfused segments (C2-C3 and C6-C7 of all FE surgical models and C4-C5 of NCZP and NCCP models), the segmental ROM was larger than that of the intact model. In flexion-extension, the ROM of the NCZP model in the nonfused C6-C7 segment was smaller than that of the other two FE models. Considering the C4-C5 segment, the ROM of the NCCP model was significantly larger than that of the NCZP model. Similar results were achieved for other actions. Accordingly, in the nonfused segments, the ROM of the NCZP model was the smallest, and the ROM of the CCP model was the largest.

Figure 4.

ROM of intact model and surgical models in flexion, extension, lateral bending, and axial rotation.

Stress Distribution of the Fusion System After ACDF

The von Mises stress distributions of the fusion devices in the FE model are shown in Fig. 5. In all actions, the stress of the Zero-P device used in the NCZP model was always higher than that of the CP device used in other surgical models, and reached a maximum value of 174.60 MPa during extension. Furthermore, the distribution of stress in the cortical bone involved in fusion (Figs. 5 and 6) was mainly concentrated in the interaction area between the screw and bone. In the FE surgical model, extension had the greatest influence on the stress of the cortical bone. Among the three fusion models, the NCZP model has the highest stress on the cortical bone, which can reach 75.48 MPa. Accordingly, the stress on the cortical bone in multiple fused segments of the NCCP model was the lowest.

Figure 5.

Maximum von Mises stress of cortical bone, implant, cartilage endplate, and IDP of each segment.

Figure 6.

Cortical bone stress distribution in three surgical models. EX indicates extension; FL, flexion; LAR, left axial rotation; LB, left lateral bending; RAR, right axial rotation; RB, right lateral bending.

IDP in the Adjacent Level After ACDF

The maximum IDP values of the NCZP, NCCP, and CCP FE models are listed in Fig. 5. Compared with that in the intact model, the maximum value of the IDP at the adjacent segments increased in all three FE surgical models. Further, the IDP of the NCZP model in most nonfused segments was smaller than that of the other FE surgical models, whereas the IDP of the CCP model increased significantly during extension and rotation motion. In addition, among all the FE surgical models, compared with the complete model, the extension had the greatest impact on the IDP of the adjacent segments. The IDP distribution features of adjacent segments in all FE models under flexion, extension, axial rotation, and lateral bending conditions are presented in Figs. 5 and 7.

Figure 7.

Nucleus pulposus stress distribution in three surgical models. EX indicates extension; FL, flexion; LAR, left axial rotation; LB, left lateral bending; RAR, right axial rotation; RB, right lateral bending.

Endplate Stress in the Adjacent Level After ACDF

As shown in Fig. 5, compared with the intact model, the maximum cartilage endplate stresses at the adjacent segments increased in the NCZP, NCCP, and CCP models. Similar to the results of the IDP in adjacent segments, the NCZP model had the lowest stress increase in the C3 superior endplate and the C6 inferior endplate during multiple actions, while the stress of the NCCP and CCP models increased significantly. In the C4 inferior endplate and C5 superior endplate, the increased stress values of the NCZP model were also lower than those of the NCCP model.

DISCUSSION

In recent years, with the advancement of finite element techniques, the development of realistic bone models directly from medical images such as CT and MRI scans, coupled with the generation of remaining component models through parameterization methods, has yielded finite element models that balance accuracy and simplicity. These models have gradually been applied in various biomechanical studies of the spine.²⁷ Currently, finite element methods are applicable for analyzing the pathogenesis of cervical spine diseases,^28,29 the biomechanical principles of various cervical spine surgeries, to determine individualized treatment plans, and to assess treatment outcomes.^29,30 Kumaresan et al²⁸ successfully simulated three different degenerative states of cervical intervertebral disks, namely mild, moderate, and severe degeneration, using a three-dimensional finite element model. They found a direct correlation between the generation of cervical osteophytes and the severity of degeneration of cervical intervertebral disks caused by prolonged excessive pressure within the vertebral bodies. Lopez-Espina et al²⁹ demonstrated through finite element analysis that sustained load loading can directly accelerate cervical intervertebral disk degeneration and the formation of vertebral osteophytes. Li et al,³⁰ in their biomechanical study of the Zero-P device using finite element analysis, showed that in single-level ACDF, the stress increment in the endplate and intervertebral disk in the ZP model was slightly lower than that in the CP model. Yu et al³¹ analyzed the biomechanical effects of different types of C5-6 interbody implants on the fusion segment using finite element analysis and found significant differences in the outcomes of different types of implants. In this study, the biomechanical properties of three surgical models were investigated using the FE method, and in the simulations, three surgical models (NCZP, NCCP, and CCP) were employed. Accordingly, the kinematic changes and stress distributions were estimated during flexion, extension, axial rotation, and lateral bending to identify the optimal type of surgical procedure for better biomechanical stability and a lower rate of complications.

ACDF procedure changes the biomechanical environment of the cervical spine.^6,32,33 In the surgical segment, the stress on the cervical spine is mainly distributed on the side of the fusion system and concentrated around the screw.³⁴ In our study, the maximum von Mises stress of the cortical bone in the NCZP appeared in the process of extension, which was lower than the strength of the cortical bone (75.48 MPa vs. 90–200 MPa).³⁰ However, our FE study simulates the stress of the cervical spine considering a fixed load, whereas it might be subjected to a greater force in daily activities³⁵; therefore, this may influence the possibility of cortical bone fractures. Similar to the stress of the cortical bone, the maximum stress of the Zero-P device was higher than that of the CP device for most activities. (Fig. 6) To explain this difference, we abstracted the fused C3-C4 CP surgical model (Fig. 8A) and the Zero-P surgical model (Fig. 8B) as mechanical models from the perspective of structural mechanics. As the interaction between the implant and vertebra is a binding connection, the fusion device can be regarded as fixed. Considering this, when the cervical vertebra is subjected to axial pressure, it will be transmitted to the screw. Because the structure is in a balanced state, the screw acts to produce a reaction force (Fig. 8). Further, F1 is proportional to the axial pressure (Fig. 8A), and F2 is proportional to the ratio of the axial pressure to cos θ (Fig. 8B); thus, the stress of the Zero-P device is greater. Although the stress of the Zero-P device reaches a maximum of 174.6 MPa during extension, it is still lower than the fatigue strength (310–610 MPa) and yield strength (789–1013 MPa) of titanium.^36,37

Figure 8.

Simplified force analysis diagram of the (A)cage plate and (B)Zero-P models in flexion.

To reduce the potential plate-related complications such as anterior soft tissue injury and dysphagia, Zero-P has been gradually applied to CDDD.¹⁴ In most clinical studies, the incidence of ASD in the Zero-P group is significantly lower than that in the CP group.^3,14 In addition, the kinematic simulation of a single segment by Li et al¹⁹ also showed that the increased ROM of the adjacent segments in the Zero-P model was lower than that in the CP model. This was similar to the results of the FE analysis. As shown in Fig. 9 (a simplified sagittal diagram of three postoperative models), the total fixed length in the postoperative model was set to Δ X (Δ X = Δ X1 + Δ X2 + …. Δ Xn), and it can be observed that Δ Xa < ΔXB < Δ Xc. Further, the total length of fixation in the NCZP model was smaller than that in the other two models, whereas the total length of fixation in the CCP model was significantly larger than that in the other two models. This means that, if the cervical vertebrae are to achieve the same ROM, the model with a larger total fixed length needs to receive more compensation in the adjacent segments. Accordingly, in the NCZP and NCCP of this study, the ROM increments of the superior, inferior, and intermediate segments (IS) of the NCZP model were lower than those of the NCCP model in many actions. We believe that compared with Zero-P, the plate limits the ROM of the fused segment to a greater extent and compensates for the ROM of the adjacent segments, especially in the flexion-extension and lateral bending directions. In terms of the IDP, the stress increment of the NCZP model was the smallest, whereas those of the NCCP and CCP models were larger (Fig. 7). The increased mechanical load promotes the adjacent intervertebral disk degenerative cascade by initiating degeneration and regulating the cell-mediated mechanisms.^38,39 In addition, the endplates play an important role in the development of intervertebral disk degeneration. Owing to the greater abnormal stress on the endplate in the CP model, it is more likely to cause dysfunction of the nutrient channel of the cartilage endplate, which might be one of the reasons for the higher incidence of ASD in the CP group.³⁵

Figure 9.

Simplified sagittal diagram of (A) NCZP, (B) NCCP, and (C) CCP model in flexion.

The routine operation for patients with discontinuous two-segment CDDD is independent of two-level discectomy and plate fixation to preserve the ROM of the intervertebral disk.⁷ However, in clinical practice, considering the natural degeneration of the intervertebral disk in the nonfusion segment and the increased abnormal stress in the IS after the operation, some doctors choose to perform three-level ACDF, including the IS, and fix the cervical vertebra with a longer plate to avoid reoperation.^6,40 In a cadaveric cervical vertebra model, Finn et al⁶ found that the ROM of the IS after fixation of two nonadjacent segments (C4-C5 and C6-C7) was significantly higher than that of an intact spine. This is similar to the kinematic simulation results in our study. In this regard, considering the ROM of the intermediate nonfusion segment (C4-C5) of the NCCP and CCP models in flexion-extension, the ROM of the NCCP model was 10.27° and that of the CCP model was only 0.26°. However, considering the superior (C3-4) and inferior (C6-7) segments of the 2-level and 3-level models, we found that in multiple actions, the ROM of the 3-level model in these two adjacent segments is larger than that of the 2-level model, such as in flexion-extension, rotation, and lateral bending. Accordingly, the ROM values of the superior adjacent segments of the CCP model were 20.1% and 12.9% larger than those of the NCCP, respectively. Lu et al⁷ treated 24 patients with discontinuous-level ACDF and CPs. Accordingly, two patients had anterior osteophyte formation in the adjacent segments, one in the IS and one in the superior adjacent segment. In a similar retrospective study by Zhang et al,⁴⁰ 14.3% (3/21) of patients had degeneration of the inferior and superior adjacent segments, and only 5% (1/21) of patients had adjacent segmental degeneration of the IS. This suggests that in addition to the IS, the superior and inferior adjacent segments of the fused segments have a risk of ASD, while the fusion fixation of more segments will further increase the range of action and mechanical load of the rest of the nonfused segments.^3,14,41,42 In clinical practice, when skip-level CDDD is encountered, it is reasonable to consider noncontiguous fusion, and choosing the Zero-P device may further reduce the risk of ASD.

Limitations

This study had some limitations. Although extra care was taken in the process of model design and motion analysis, FE analysis had some innate limitations. First, a complete cervical vertebral FE model was based on a single CT scan of a normal individual, and on this basis, a fusion model was created. Therefore, the analyzed fusion data might not represent the entire population. However, the overall trend represented by the finite element is reliable. Second, model verification was based on the study of cadaveric specimens, which is not completely consistent with real-world situations. In addition, vertebral osteoporosis and degenerative changes of the intermediate segment were not considered in the construction of the FE model. Finally, only linear elastic materials were used for the vertebral body and the intervertebral disk. However, the main conclusions of this paper were based on the comparative analysis among the three models, thereby being less influenced by the aforementioned simplifications. Accurate data need to be further combined with biomechanical tests. Further research is needed to explore the long-term biomechanical changes in the cervical spine.

CONCLUSION

Noncontiguous ACDF with Zero-P provides more reliable biomechanical stability for patients because of its minimal impact on the cervical biomechanical environment. In addition, the use of Zero-P devices can reduce the stress on adjacent intervertebral disks and endplates, resulting in a reduced risk of ASD development. However, the high cortical bone stress caused by the Zero-P device may influence the risk of fractures.

Key Points

• Noncontiguous anterior cervical discectomy and fusion with Zero-P provides reliable stability.

• The use of Zero-P can reduce the stress on adjacent intervertebral disks and endplates.

• The use of Zero-P devices results in a reduced risk of ASD. However, the high cortical bone stress caused by the zero-profile device cannot exclude the risk of fractures.